Pathological aspects of breast cancer in Indonesian females, emphasizing on the modified W.H.O. classifïcation
156
Tjahjadi et al.
Med J Indones
Pathological Aspects of Breast Cancer in Indonesian Females, Emphasizing
on the Modified W.H.O. Classifïcation
Gunawan TJahj
e$, Joedo Prihartonol l,
,
Yoshiyuki Ohn
Much-lis Ramli+,
,
Idral Darwisr,
i
Abstrak
Angka kejadian kanker payudara sangat bervariasi di antara berbagai daerah geografik dan perbedaan perangai patologik serta aspek
biologik mungkin menyebabkan perilaku klinik yang berbeda pada penyakit tersebut. Pada penelitian ini kami bermaksud. meneliti
persamaan dan perbedaan perangai histopatologik kanker payudara antara wanita Indonesia dan wanita Jepang. Tiga ratus kasus
kanker payud,ara yang diobati di Rumah Sakit Umum Pusat Cipto Mangunkusumo (RSCM), Jakarta, Ind.onesia, selama 3 tahun
(1988-1991), diteliti aspek histopatologinya. Sediaan-sediaan dianalisa dengan menggunakan klasifikasi yang dianjurkan oleh
'lapaneseBreastCancerSociety". Hasilnyadibandingkandengandatayangdiperolehdari446kasuspada"CancerlnstituteHospital"
(CIH), Tolryo, Jepang. Pada kasus kanker payudara di RSCM ditenukan 1.33 Vo karsinoma non-invasif, 88.3 Vo karsinoma duktal invasif
dan 9.7 Vo tipe khusus. Data kanker payudara di CIH menunjukkan 7.4 Vo karsinoma non-invasiJ 80.4 Vo karsinoma d.uhal invasif dan
11.3 % tipe l:husus. Jumlah penderita kanker payudara Indonesiapada golonganusia 20-29 tahuntampak lebih tinggi d.aripadawanita
Jepang. Pada kedua penelitian tersebut jumlah kanker payudara terbanyak pada golongan usia 40-49 tahun. Tumor yang ditemukan
pada wanba Indonesia mempunyai ukuran yang lebih besar daripada wanita Jepang. Proporsi karsinoma musinosum dan karsinoma
Iobularis l"ebih tinggi pada wanita Jepang, sedangkan proporsi karsinoma medularis lebih linggi pada wanita Indonesia.
Ab.stract
The incidence of breast cancer varies greatly amonç geographic regions and differences in pathological patterns and biological aspecls
might result in different clinical behavior of the disease. In this stud,y we would. like to investigate the similarity and dissimilarity of
hislopathological patterns of breast cancer among the Indonesian and the J apanese females. Three hundred cases of breast carcinoma
treated at Dr. CiptoMangunkusumoHospital (RSCM), Jakarta, within 3 years (1988-1991) were analysedfor thevarious histophatological aspects. The specimens were reviewed using the classificalion recommended by the Japanese Breast Cancer Society. We also
compared with the data of 446 Japanese breast cancer cases from the Cancer Institute Hospital (CIH), Tolqo, Japan. The RSCM cases
had 1,33Vo noninvasive carcinoma, 88,3Vo kvasive carcinoma and 9,67Vo special types. The CIH cases were 7,4Vo noninvasive
carcinoma, 80,4Vo invasive ductal carcinoma and, 11,3Vo special types. Compared to the Japanese females ir was noticed that breast
cancer cases had already occured more frequently at the younger age Broup (20-29 years) of the I ndonesian femal.es. However, the uge
distributions ofboth groups peaked at 40-49 years. Indonesianfemales had larger-sized tumors. The proportion of mucinous and lobular
carcinomas were higher in Japanese females, while the proportion of medullary carcinoma was higher in Indonesian females.
Key wotds: breast cancer, histopathological patterns, new classification.
*
Dqtartment of Anatomic Pathology, Faculty of Medicine IJniversity
of Indonesia, Dr. Cipto Mangunhsumo National Cenlral General
H ospila I, J aka rta I 04 j 0, I n donzsi a.
f Department of Pathology, Cancer Institute Hospital, Tokyo
170, Japan
I Deparlmen! of Surgery, FaculE of Medicine IJniversity of Indonæia,
Dr. Cipto Mangunhusumo Nationtl Cenlral General Hospital,
O,
''
n
Indonesia.
Institute Hospita!, Tolqo 170, Japan
Communily Medicine, Faculty of Medicine University
S, rgery, Cancer
oya IJniversity,Nagoya466,
..Japan.
Department of Preventive Medicine, Nagoya City University, Nagoya
467, Japan.
Breast cancer
is a world-wide, very common
and
serious disease, and comprises a relatively high incidence, namely about 2O% among all malignancy.r
It is also the commonest fatâl cancer with an incidence
of 22.2 per 100.000 person years.2 The incidence of
breast carcinoma varies greatly among geographic
regions,
it is high in European countries,
Canada,
Australia, New Zealand, similar to those of the United
Vol 4, No
j, July
some
Asia-iapan.3
cidence rate
in Japan the
States.
PathologicalAspects of Breast
- September 1995
in
n-
ut
of
breast cancer in Japan has been reported to be lower
(12.1-16 per 100.000 fernales) than in Anerica (7I.7
per 100.000 females), as stated in the Cancer incidence
in Five Continents, innC publicatiorn.3 In lndonesia,
according to the various Pathology-based cancer
registry, breast cancer ranked the second, succeeding
the cerv_ical cancer, with a relative frequency of
ll.59o/o.6
These differences has attracted several investigators to
look upon several aspects of breast cancer, with sys-
Cancer
157
METHODS
Three hundred cases of breast carcinoma were diagnosed and treated at the Dr. Cipto Mangunkusumo
National Central General Hospital (RSCM) within 3
years (1988-1991). These cases were from operable
cases and biopsy specimens only, accounting for 110
and 190 cases respectively. The size of the tumor was
the largest diameter of the tumor measured ort the cut
surface of the gross spesimen as recorded in the pathology report. Lymph-node metastases, using the "n"
classification, were grouped from n0 to n3. Based on
the histological examination of lymph nodes, they
were classified as shown in Table 1.
tematic epiderniological studies. In addition, further
comparison has been studied by analyzing the
pathological and biological aspects of the disease,
Table 1. Lymph nodes metastases classification
among American and Japanese women, and found out
that breast cancer among Japanese females is characteized _by a relatively low incidence and good prog-
"n" grouping
nosis.T'8
n0
Lymph nodes involvement
no metasiasis
In order to better understand about the disease, such
nla
1-3 positive axillary lymph nodes
comparative studies are also needed to be implemented
among Indonesian and Japanese womell. Further
analysis on histopathological features and biological
behaviour of the disease would be a great contribution
to the current methods of treatment and refinements in
therapeutic regimens.
n1b
4 or more positive axillary lymph nodes
From the pathology standpoint of view, a number of
biological factors and principles have been delineated
which pennit an increasingly accurate prediction of
prognosis and benefit of therapy, such as : histologic
type, histologic grade, tumor size and axillary lymph
node status. Breast cancer presents in a great variety of
histological patterns, including spesific types which
have useful clinical correlates and prognostic implications. There are various classifications of breast caucer, and in Indonesia we used the classification of
WHO (1981)e and that of McDivitt etal.10 Since 1989
we adoptecl ihe classification use in Japan,l1 which is
fundamentally the same as the WHO classification,
with the addition of a subclassification of the invasive
ductal carcirloma into 3 sub-types.
The purpose of this study is to analyse the various
histological variations of breast cancer in the Indonesian fernales, adjustiug it with the new classification and their frequencies, and to compare it with the
results of the Cancer lnstitute, Tokyo, Japan.
n2
metastasis in subclavicular lymph nodes
n3
metastasis in supraclavicular lymph nodes
Of the 1 10 operable cases, only in 40 cases the lymph
nodes could be analysed.
Five microns histological specimens were stained with
hematoxylin-eosin standard procedure, similarly applied in both the lndonesian and the Japanese breast
cancer specimers.
The specimens were reviewed by three investigators
(GT, ES) and (GS) during the consultation meetings,
referring to the classification recolntnended by the
Japanese Breast Cancer Society. Agreement on the
final diagnosis was established by applying the standard criteria of specific histological typing.
HISTOLOGICAL CLASSIFICATION USED IN
.IAPAN
The Japanese Breast Cancer Society
will
adopt here
after the new histological classification of breast
tumors as shown in Table 2.
158
Tjahjadi et at.
Med J Indones
2. Histological
Table
Classification ol Breast Tumors
(Japanese Breast Cbncer Society, 1984)
The most common was the invasive ductal cârcinoma
(88.33Eo), followed by the special types (9.67To), and.
the noninvasive carcinom a (1.337o). Tçwo out of three
hundred were diagnosed as Paget,s disease.
Malignant (Carcinoma)
l.
Noni nvasive carcinoma
a. Noninvasive ductal carcinoma
b. Lobular carcinoma in situ
Among the invasive ductal carcinoma
2. Invasive carcinoma
a. Invasive ductal carcinoma
al. Papillotubular carcinoma
The case distribution
given in table 4.
b. Special types
b2.
b3.
b4b5.
b6.
b7.
b8.
Mucinous carcinoma
Medullarycarcinoma
Invasive lobular carcinoma
Adenoid cystic carcinoma
Squamous cell carcinoma
Spindle cell carcinoma
Apocrine carcinoma
Age at opera ti on/bi opsy
20 -29
is
ma (Juveni le carci noma)
Vo
55
4.33
24.00
31.00
r8.33
58
19.33
9
3.00
13
72
93
60-69
70 -79
b9. Tubular carcinoma
ca rci no
Number of cases
30-39
40-49
50-59
Carcinoma with cartilaginous and or osseous
0. Secreto ry
bl l. others
by age at operation/biopsy
Table 4. Case Distribution by Age at Operation/Biopsy
metaplasia
bI
the scir-
types, the medullary carcinoma was diagnosed in
5.687o of the cases.
a2. Solid-tubularcarcinoma
a3. Scirrhous carcinoma
bl.
(à),
rhous type was the most colnmon accounted for 49To
of the cases. Among the non invasive carcinoma, no
lobular carcinoma in situ was fou;d. In the special
Totals
300
100.00
3. Paget's disease
Notes
:
See Appendix for tbe principles and details of
cl assificati on
RESULTS
The case distribution by histological type is shown in
Table 3.
Table
3.
Histological Types and Case Distriburion
Cancer (1988-1991)
Histological types
Noninvasive carcinoma
a. Noninvasive ductal ca
b. Lobular ca io situ
Invasive carcinoma
a. Invasive ductal carcinoma
a1. Papillotubular
a2. Solid-tubular
a3. Scirrhous
ol
Number of (hses
Breast
%
Mucinous carcinoma
Medullary carcinoma
Invasive lobular carcinoma
Adenoid cystic carcinoma
Paget's disease
Totals
The location of the fumor in the left breast was found
more frequent than in the right breast (see table 5), and
3.67 7o were bilateral.
Table 5. Case Distribution o[ Breast Cancer by Location
Location
Left breast
Right breast
Bilateral
4
0
t.33
Totals
Number of cases
r72
39
79
13.00
26.33
r47
49.0O
Vo
11
57.33
39.00
3.67
300
100.00
1,1,7
0.00
b. Special types
b1.
b2.
b3.
b4.
Tbe age distribution showed the youngest case of 22
years old, and the oldest was 75 years old. The peak
incidence was found in the 5th decade (3lo/o).
Only 6 of these operable cases have tumor smaller than
2 cm in diameter. Fifty five cases (50%) have tumors
more than 5 cm in diameter (see Table 6).
Table 6. Case Distribution by Sizç of Tumorassessed on
surgical specimens of operable cases
4
1.33
t7
5.68
Size of tumor
7
I
2.33
0.33
5cm
49
55
300
100.00
2.1
-5cm
Totals
Number of cases
110
%
5.5
44.5
50
100.00
Vol 4, No
j, July
Pathological Aspects of Breast
- September 1995
The case distribution by tumor size of the whole cases,
and compare with the cases from Cancer Institute
Hospital (CIH) is shown in Table 7.
Table
7.
Case Distribution by Size of Tumor according to
clinical assessment ofall breast câncer czses
Cancer
159
The data at the CIH showed that some patienis under-
went subclavicular and supraclavicular lympb node
dissections, but at the RSCM lymph node dissections
were limited to an axillary group. The rates were almost equal at the RSCM and CIH for the n0 and n1a.
The incidence for n1b was 6.10/o gteater at the RSCM.
The comparative câse distribution by histological
Size ol tumor
crH
RSCM (1e88-19er)
Number of
types is shown in Table 9.
(1eSe)
Number of
cases
%
CASES
Vo
TO
22
4.9
2
r82
40.8
5l
t7
191
42.8
87
29
4.7
T4
2l
156
52
30
6.7
Totals
300
r00
446
100
T1
T2
T3
6
The RSCM cases had 1.33% noninvasive carcinoma,
8833% invasive ductal carcinoma, and 9.67% special
types. The CIH cases had 7.47o noninvasive carcinoma, 80.47o invasive ductal carcinoma, and IL37o
special types. The noninvasive carcinoma group, no
lobular carcinoma in situ was found. The incidence of
noninvasive duct carcinoma is much higher at the ClH,
with a 6.O7Vo difference, than that at the RSCM.
Table 9. Histological Types and Case Distribution
The data showed that 52 7o of the Indonesian breast
cancer patients at Cipto Mangunkusumo Hospital
(RSCM) were at advanced stage with T4 size, while
such tumor was only found in 6.7Vo among the
Japanese breast cancer patients at CIH. On the contrary early breast cancers with T1 size were only seen
in2% of the Indonesian females, while it was found in
40.8% of the Japanese females.
At RSCM, the rnajority (rnore than 807o) were of
T3+T4 size, while at CIH the majority (rnore than
8O7o) were of T1+T2 size. In other words, at their
presentatiol the tumor size of breast cancer among
Indonesian females were larger than that alnong
Japanese females.
ln forty of the operable cases, the lymph node metastases could be analysed. The results are given in
Table 8.
Table 8. Case Distribution by Lymph-node Metastases
RSCM
(1e88-1eer)
CrH (lq8e)
Lympb-node metastases
Number of
cases
7o
Number of
cases
%
Negative (n0)
22
55
229
51.3
Axillary
l0
25
133
29.8
8
20
62
13.9
l5
3.4
7
1.6
1-3
(nla)
Axillary 4 or more (nlb)
Subclavicular (n2)
Supraclavicular (n3)
Totals
40
100
446
100
RSCM (1e88-1ee1) CrH (1e89)
Histological types
Number of
cases
Noninvasive carcinoma
a. Noninvasive ductal ca
b. Lobular ca in situ
Invasive carcinoma
a. lnvasive ductal ca
a1. Papillotubular
a2- Solidtubular
a3. Scirrbous
4
Mucinous ca
b2.
b3.
b4.
b5.
b6.
b7.
b8.
Medullary
ca
Invasive lobular ca
Adenoid cysticca
cases
r.33 33
4
t7
'l
1
1.33 t6
5.68 6
2.33 20
Vo
7.4
r9.3
17.5
43.6
3.6
1.3
4.5
0.33
Squamous cell ca
1
0.2
0.2
0.2
5
1.1
1
Spindle cell ca
Apocrine ca
Cla
Number of
39 13.00 86
79 26.33 78
t47 49.00 t94
b. Special types
bl.
%
1
with cartil and/or
oss. metaplasia
b9. Tubular
ca
blO.Secretory ca
(Juvenile)
Paget's disease
Tota s
07
0.67
300
100.00
445
100.0
160
Tjahjadi et al.
Med J Indones
DISCUSSION
approximately 2Vo. At the RSCM
It was of great concern, that the majority of the Indonesian breast cancers found at their presentation
were of much later stages in contrast to the Japanese
counterpart.
The earlier detection of breast caucer could be responsible for the difference shown in Table 9 for the
non-invasive types. In the invasive cârcinoma group,
the invasive ductal carcinorna is the most common,
accounting for at least 8O7o of breast cancer. The
incidence of 88.337o at the RSCM is similar with the
report of Sakamoto et al.? The scirrhous carcinoma is
the most common type of invasive ductal carcinoma,
with an incidence ol about S}Vo.rz The data of the
Indonesian breast cancers showed that the proportion
of the solid-tubular carcinoma was higher than
the
papillotubular carcinoma, while the reverse was seen
in the data of tbe Japauese breast cancer.
The sub-classification of invasive ductal carcinoma
into 3 sub-types has prognostic significance. Such
relationship has been observed by several investigators
(Sakamoto G., personal communication). The papillotubular carcinoma shows the most favorable prog-
nosis (ten-year survival rate = 77.4 %), and the
scirrhous carcinorna shows the worst prognosis (tenyear survival rate = 61.2 o/o). The solid-tubular carcinoma showed a ten-year survival rate of 64.9 7o.T\e
invasive ductal carcinorna has been referred to as
infiltrating duct carcinoma not otherwise specified
(NOS) or no special type (NST). This group of carcinoma which is usually evaluated
c grad-
ing,13' 1a which
will place th
intermediate or high grade ca
s into
This
proposed new histologic al classification can be used
instead of the grading system.
The special types of invasive breast cancer, including
mucinous carcinoma, rnedullary carcinoma, tubular
carcinoma in their pure form (more than 90o/o
homog,e.ueity) have relatively favourable prognosis.*'" Although invasive, these tumors show a low
incideuce of axillary lyrnph-nocle_lnetastases and exhibit a Iong disease free interval.r /'lu
the CIH, it is 3.67o.
itis
l.33Vo, and at
An interesting finding is that medullary carcinoma at
the RSCM has a much higher incidence rate than that
at the CIH, with a difference of 4.38%. Such type has
been considered to represent more favourable prognosis.
The incidence of lobular carcinoma in Japan is very
low and is significa_ntly different from the incidence in
Western countries./ However Sugano and Sakamoto20
found that the incidence of lobular carcinoma among
Japanese females has gradually increased. At the CIH
before 1965,the incidence was around l7o of allbreast
cancers, from l97l to 1975 it was 3.4To, and, mosl
recently, for 1974-1975, it has increased to 5.3To.They
concluded that the incidence of invasive lobular carcinoma among Japanese females is gradually approaching that of American females.
In 1989, the incidence of invasive lobular carcinoma
at CIH was 4.57o. At the RSCM, the incidence of
invasive lobular carcinoma for 1981-1985 was 1.77o
among 1265 cases of breast cancer,zr and in this study
(1989-1992), it accounted for 2.33% among 300 cases
of breast cancers.
No tubular carcinoma was found among the RSCM
cases, but 5 cases were detected among the CIH cases
of breast cancer. Tubular carcinomas are well differen-
tiated tumors which show the highest rate of cure,
among the special histologic typ;.22,23 Tubular carcinoma has received general recognition only in the
last 10 years, since it is more common in groups of
cancer detected by mammography, largely explaining
the increased interest in recent years.to This special
type of breast cancer are more frequent in prevalent
caucer (those detected at first screen by mammography) than cases detected subsequently at yearly intervals (incident cases)." Whether this is true for the
CIH cases is worthwile to be elucidatecl.
investigators estimated that special type cancer comprise lOTo of all breast cancers, while others considered
that they comprised between 25-30Vo.r6
The peak incidence ofbreast cancer among Indonesian
females was found in the 5th decade, and was similar
with the result at the CIH cases. The main difference
with reference to the age distribution of breast carcinoma between Indonesia and Japanese females was
inthe20-29 year agegroup. Thirteen cases were founcl
âmong 300 breast cancer cases at the RSCM, while
only 2 cases among Japanese females with breast cancer, in the 2O-29 year age group. It seems that breast
Mucinous carcinoma comprised_ only l-6%o of most
series of invasive breast crucer,t'and the pure type
douesian females.
In both studies (RSCM and CIH) the ilcidelce of this
special type is only about lÙt/o of the whole breast
caucer cases. This finding is similar with previous
report by Sakamoto et al.' In North America, some
cancer occurs at the younger age group
in the
In_
Vol 4, No 3, July - September 1995
Pathological Aspects of Breast
CONCLUSIONS
Cancer
16f
8. Rosen PP, Ashikari R, Thaler H, Ishikawa S, Hirota T, Abe
O, et al. A comparative study of some pathological features
of mammary carcinoma in Tokyo, Japan and New York,
USA. Ca ncer I97 7 ;39 :429 -3 4.
9. Hartmann WH, Ozello L, Sobin LH, Stalsberg H. Histological typing of breast tumoum. In : International Histological
Classification of Tumours, no 2.2nd ed. Geneva : WHO,
At younger age group QO-29 years), breast cancer had
already occured more frequently in the lndonesian
females as compared to the Japanese females. However, the age distribution in both groups peaked at ages
40-49 years. Indonesian females had larger-sized
tumors. The proportion of non-invasive carcinoma
was lower among Indonesian females, while that of
invasive ductal carcinoma was comparable in both
10. Modivitt RW, Stewart FW, Berg JW. Tumours of the breast.
ln: Atlas of Tumor Pathology. 2nd series. Washington DC:
was of great interest, that medullary carcinoma, which
11. Japanese Breast Cancer Society. The Geneial Rules for
Clinical and Pathological Recording ofBreast Cancer. Jpn J
groups. Tbe proportion of mucinous carcinoma,
lobular carcinoma were higher in Japanese females. It
has more favourable prognosis, occured
higher proportion in Indonesian females.
in much
Acknowledgments
The authors are indebted to the nurses and laboratory
technicians for excellent care of surgicopathological
specimens. This work was supported by the Ministry
of Education and Culture, Japan, Grants No.01042007
and 04042013; and was partly supported by the Indonesian Cancer Foundation. This collaborative study
was a part of Special Cancer Research Project in Monbusho International Scientific Research Program, with
the approval of the Dean, Faculty of Medicine, University of Indonesia, No. 4383 /PTO2.H4.FK / E / 88.
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Appendix
part. Comedocarcinoma belongs to this
type.
A. Principles of Classification
1.
Breast carcinoma is classified into three groups;
noninvasive ca rci noma, i nvasive ca rcinoma a nd
Paget's disease.
2.
Noninvasive carcinoma is classified into noninvasive ductal carcinoma and lobular carcinoma
in situ; Invasive carcinoma into invasive ductal
carcinoma and special types.
3.
Invasive ductal carcinoma is further classified
into three subgroups; papillotubu lar carcinoma,
solid-tubular carcinoma and scirrhous carcinoma.
Remark 1: Comedocarcinoma should be
identified as that.
Remark 2: Papillary carcinoma which is an
independent histological type in
the WHO classification has been
included in papittotubular carcinoma.
However there is still room for
further consideration.
à2. Solid+ubular
Note : since this type is characterized
by distinct bounderies, tumors
Invasive carcinoma
This group represents a carcinoma with in-
composed of medullary and/or
solid nests are also included,
vasion.
à.
carcinoma
This is a carcinoma characterized by a
solid cluster of cancer cells with expansive growth forming sharp borders.
B. Definition of Histological Types
2.
J Univ Indones
Invasive ductal carcinoma
if
This is classified into rhree subgroups;
even
cinoma and scirrhous carcinoma.
Classification of invasive carcinoma fol-
Central necrosis or fibrosis may
also be evident.
papillotubular carcinoma, solid-tubular car-
lows the rule of predominancy when there
are two or more histological patterns. In a
case where judgement of the predominant
type is difficult, the least differentiated type
should be chosen as the histological type,
with supplementary description of other histological types.
Remark 1: In practice, the predominant his-
tological type should be taken
for the principal classification,
and the secondary histological
type should be added as â sup-
plementary description.
Remark 2: The degree
of differentiation
from poor to well is in order of
scirrhous carcinorna, solidtubular carcinoma and papillotubular carcinoma.
Remark
3: A lesion with slight extraductal
invasion should be so described
for easier correspondence with
the WHO classification.
à l.
Papillotubular carcinorna
This carcinoma is characterized by
papillary projection and tubule formation, and may contain a solid pattenr in
interstitial components
of stromal tissue are
à3.
present.
Scirrhous carcinoma
Cancer cells
of this histologic
type
show scattered invasion into the stroma
in small clusters or in trabecular structures with accompanying desmoplasia
of varying degrees.
there are two subtypes. One is a pure
scirrhous carcinoma which has extremaly small amount of intraductal
component and extersive stromal invasion. The other derives from papillotubular or solid-tubular carcinoma
with a predominance of diffuse stromal
invasion.
Note :The differential diagnosis between scirrhous carcinoma and
solid-tubular carcinoma relies
on the size of cancer flests and
the fashion of infiltration at the
tumor margin. Scirrhous carcinoma is composed of small
nests, grows diffusely and infiltrates into the stromal tissue.
On the other hand, solid-tubular
carcinoma has large nests,
grows expansively and is well
circumscribed.
Tjahjadi et al.
Med J Indones
Pathological Aspects of Breast Cancer in Indonesian Females, Emphasizing
on the Modified W.H.O. Classifïcation
Gunawan TJahj
e$, Joedo Prihartonol l,
,
Yoshiyuki Ohn
Much-lis Ramli+,
,
Idral Darwisr,
i
Abstrak
Angka kejadian kanker payudara sangat bervariasi di antara berbagai daerah geografik dan perbedaan perangai patologik serta aspek
biologik mungkin menyebabkan perilaku klinik yang berbeda pada penyakit tersebut. Pada penelitian ini kami bermaksud. meneliti
persamaan dan perbedaan perangai histopatologik kanker payudara antara wanita Indonesia dan wanita Jepang. Tiga ratus kasus
kanker payud,ara yang diobati di Rumah Sakit Umum Pusat Cipto Mangunkusumo (RSCM), Jakarta, Ind.onesia, selama 3 tahun
(1988-1991), diteliti aspek histopatologinya. Sediaan-sediaan dianalisa dengan menggunakan klasifikasi yang dianjurkan oleh
'lapaneseBreastCancerSociety". Hasilnyadibandingkandengandatayangdiperolehdari446kasuspada"CancerlnstituteHospital"
(CIH), Tolryo, Jepang. Pada kasus kanker payudara di RSCM ditenukan 1.33 Vo karsinoma non-invasif, 88.3 Vo karsinoma duktal invasif
dan 9.7 Vo tipe khusus. Data kanker payudara di CIH menunjukkan 7.4 Vo karsinoma non-invasiJ 80.4 Vo karsinoma d.uhal invasif dan
11.3 % tipe l:husus. Jumlah penderita kanker payudara Indonesiapada golonganusia 20-29 tahuntampak lebih tinggi d.aripadawanita
Jepang. Pada kedua penelitian tersebut jumlah kanker payudara terbanyak pada golongan usia 40-49 tahun. Tumor yang ditemukan
pada wanba Indonesia mempunyai ukuran yang lebih besar daripada wanita Jepang. Proporsi karsinoma musinosum dan karsinoma
Iobularis l"ebih tinggi pada wanita Jepang, sedangkan proporsi karsinoma medularis lebih linggi pada wanita Indonesia.
Ab.stract
The incidence of breast cancer varies greatly amonç geographic regions and differences in pathological patterns and biological aspecls
might result in different clinical behavior of the disease. In this stud,y we would. like to investigate the similarity and dissimilarity of
hislopathological patterns of breast cancer among the Indonesian and the J apanese females. Three hundred cases of breast carcinoma
treated at Dr. CiptoMangunkusumoHospital (RSCM), Jakarta, within 3 years (1988-1991) were analysedfor thevarious histophatological aspects. The specimens were reviewed using the classificalion recommended by the Japanese Breast Cancer Society. We also
compared with the data of 446 Japanese breast cancer cases from the Cancer Institute Hospital (CIH), Tolqo, Japan. The RSCM cases
had 1,33Vo noninvasive carcinoma, 88,3Vo kvasive carcinoma and 9,67Vo special types. The CIH cases were 7,4Vo noninvasive
carcinoma, 80,4Vo invasive ductal carcinoma and, 11,3Vo special types. Compared to the Japanese females ir was noticed that breast
cancer cases had already occured more frequently at the younger age Broup (20-29 years) of the I ndonesian femal.es. However, the uge
distributions ofboth groups peaked at 40-49 years. Indonesianfemales had larger-sized tumors. The proportion of mucinous and lobular
carcinomas were higher in Japanese females, while the proportion of medullary carcinoma was higher in Indonesian females.
Key wotds: breast cancer, histopathological patterns, new classification.
*
Dqtartment of Anatomic Pathology, Faculty of Medicine IJniversity
of Indonesia, Dr. Cipto Mangunhsumo National Cenlral General
H ospila I, J aka rta I 04 j 0, I n donzsi a.
f Department of Pathology, Cancer Institute Hospital, Tokyo
170, Japan
I Deparlmen! of Surgery, FaculE of Medicine IJniversity of Indonæia,
Dr. Cipto Mangunhusumo Nationtl Cenlral General Hospital,
O,
''
n
Indonesia.
Institute Hospita!, Tolqo 170, Japan
Communily Medicine, Faculty of Medicine University
S, rgery, Cancer
oya IJniversity,Nagoya466,
..Japan.
Department of Preventive Medicine, Nagoya City University, Nagoya
467, Japan.
Breast cancer
is a world-wide, very common
and
serious disease, and comprises a relatively high incidence, namely about 2O% among all malignancy.r
It is also the commonest fatâl cancer with an incidence
of 22.2 per 100.000 person years.2 The incidence of
breast carcinoma varies greatly among geographic
regions,
it is high in European countries,
Canada,
Australia, New Zealand, similar to those of the United
Vol 4, No
j, July
some
Asia-iapan.3
cidence rate
in Japan the
States.
PathologicalAspects of Breast
- September 1995
in
n-
ut
of
breast cancer in Japan has been reported to be lower
(12.1-16 per 100.000 fernales) than in Anerica (7I.7
per 100.000 females), as stated in the Cancer incidence
in Five Continents, innC publicatiorn.3 In lndonesia,
according to the various Pathology-based cancer
registry, breast cancer ranked the second, succeeding
the cerv_ical cancer, with a relative frequency of
ll.59o/o.6
These differences has attracted several investigators to
look upon several aspects of breast cancer, with sys-
Cancer
157
METHODS
Three hundred cases of breast carcinoma were diagnosed and treated at the Dr. Cipto Mangunkusumo
National Central General Hospital (RSCM) within 3
years (1988-1991). These cases were from operable
cases and biopsy specimens only, accounting for 110
and 190 cases respectively. The size of the tumor was
the largest diameter of the tumor measured ort the cut
surface of the gross spesimen as recorded in the pathology report. Lymph-node metastases, using the "n"
classification, were grouped from n0 to n3. Based on
the histological examination of lymph nodes, they
were classified as shown in Table 1.
tematic epiderniological studies. In addition, further
comparison has been studied by analyzing the
pathological and biological aspects of the disease,
Table 1. Lymph nodes metastases classification
among American and Japanese women, and found out
that breast cancer among Japanese females is characteized _by a relatively low incidence and good prog-
"n" grouping
nosis.T'8
n0
Lymph nodes involvement
no metasiasis
In order to better understand about the disease, such
nla
1-3 positive axillary lymph nodes
comparative studies are also needed to be implemented
among Indonesian and Japanese womell. Further
analysis on histopathological features and biological
behaviour of the disease would be a great contribution
to the current methods of treatment and refinements in
therapeutic regimens.
n1b
4 or more positive axillary lymph nodes
From the pathology standpoint of view, a number of
biological factors and principles have been delineated
which pennit an increasingly accurate prediction of
prognosis and benefit of therapy, such as : histologic
type, histologic grade, tumor size and axillary lymph
node status. Breast cancer presents in a great variety of
histological patterns, including spesific types which
have useful clinical correlates and prognostic implications. There are various classifications of breast caucer, and in Indonesia we used the classification of
WHO (1981)e and that of McDivitt etal.10 Since 1989
we adoptecl ihe classification use in Japan,l1 which is
fundamentally the same as the WHO classification,
with the addition of a subclassification of the invasive
ductal carcirloma into 3 sub-types.
The purpose of this study is to analyse the various
histological variations of breast cancer in the Indonesian fernales, adjustiug it with the new classification and their frequencies, and to compare it with the
results of the Cancer lnstitute, Tokyo, Japan.
n2
metastasis in subclavicular lymph nodes
n3
metastasis in supraclavicular lymph nodes
Of the 1 10 operable cases, only in 40 cases the lymph
nodes could be analysed.
Five microns histological specimens were stained with
hematoxylin-eosin standard procedure, similarly applied in both the lndonesian and the Japanese breast
cancer specimers.
The specimens were reviewed by three investigators
(GT, ES) and (GS) during the consultation meetings,
referring to the classification recolntnended by the
Japanese Breast Cancer Society. Agreement on the
final diagnosis was established by applying the standard criteria of specific histological typing.
HISTOLOGICAL CLASSIFICATION USED IN
.IAPAN
The Japanese Breast Cancer Society
will
adopt here
after the new histological classification of breast
tumors as shown in Table 2.
158
Tjahjadi et at.
Med J Indones
2. Histological
Table
Classification ol Breast Tumors
(Japanese Breast Cbncer Society, 1984)
The most common was the invasive ductal cârcinoma
(88.33Eo), followed by the special types (9.67To), and.
the noninvasive carcinom a (1.337o). Tçwo out of three
hundred were diagnosed as Paget,s disease.
Malignant (Carcinoma)
l.
Noni nvasive carcinoma
a. Noninvasive ductal carcinoma
b. Lobular carcinoma in situ
Among the invasive ductal carcinoma
2. Invasive carcinoma
a. Invasive ductal carcinoma
al. Papillotubular carcinoma
The case distribution
given in table 4.
b. Special types
b2.
b3.
b4b5.
b6.
b7.
b8.
Mucinous carcinoma
Medullarycarcinoma
Invasive lobular carcinoma
Adenoid cystic carcinoma
Squamous cell carcinoma
Spindle cell carcinoma
Apocrine carcinoma
Age at opera ti on/bi opsy
20 -29
is
ma (Juveni le carci noma)
Vo
55
4.33
24.00
31.00
r8.33
58
19.33
9
3.00
13
72
93
60-69
70 -79
b9. Tubular carcinoma
ca rci no
Number of cases
30-39
40-49
50-59
Carcinoma with cartilaginous and or osseous
0. Secreto ry
bl l. others
by age at operation/biopsy
Table 4. Case Distribution by Age at Operation/Biopsy
metaplasia
bI
the scir-
types, the medullary carcinoma was diagnosed in
5.687o of the cases.
a2. Solid-tubularcarcinoma
a3. Scirrhous carcinoma
bl.
(à),
rhous type was the most colnmon accounted for 49To
of the cases. Among the non invasive carcinoma, no
lobular carcinoma in situ was fou;d. In the special
Totals
300
100.00
3. Paget's disease
Notes
:
See Appendix for tbe principles and details of
cl assificati on
RESULTS
The case distribution by histological type is shown in
Table 3.
Table
3.
Histological Types and Case Distriburion
Cancer (1988-1991)
Histological types
Noninvasive carcinoma
a. Noninvasive ductal ca
b. Lobular ca io situ
Invasive carcinoma
a. Invasive ductal carcinoma
a1. Papillotubular
a2. Solid-tubular
a3. Scirrhous
ol
Number of (hses
Breast
%
Mucinous carcinoma
Medullary carcinoma
Invasive lobular carcinoma
Adenoid cystic carcinoma
Paget's disease
Totals
The location of the fumor in the left breast was found
more frequent than in the right breast (see table 5), and
3.67 7o were bilateral.
Table 5. Case Distribution o[ Breast Cancer by Location
Location
Left breast
Right breast
Bilateral
4
0
t.33
Totals
Number of cases
r72
39
79
13.00
26.33
r47
49.0O
Vo
11
57.33
39.00
3.67
300
100.00
1,1,7
0.00
b. Special types
b1.
b2.
b3.
b4.
Tbe age distribution showed the youngest case of 22
years old, and the oldest was 75 years old. The peak
incidence was found in the 5th decade (3lo/o).
Only 6 of these operable cases have tumor smaller than
2 cm in diameter. Fifty five cases (50%) have tumors
more than 5 cm in diameter (see Table 6).
Table 6. Case Distribution by Sizç of Tumorassessed on
surgical specimens of operable cases
4
1.33
t7
5.68
Size of tumor
7
I
2.33
0.33
5cm
49
55
300
100.00
2.1
-5cm
Totals
Number of cases
110
%
5.5
44.5
50
100.00
Vol 4, No
j, July
Pathological Aspects of Breast
- September 1995
The case distribution by tumor size of the whole cases,
and compare with the cases from Cancer Institute
Hospital (CIH) is shown in Table 7.
Table
7.
Case Distribution by Size of Tumor according to
clinical assessment ofall breast câncer czses
Cancer
159
The data at the CIH showed that some patienis under-
went subclavicular and supraclavicular lympb node
dissections, but at the RSCM lymph node dissections
were limited to an axillary group. The rates were almost equal at the RSCM and CIH for the n0 and n1a.
The incidence for n1b was 6.10/o gteater at the RSCM.
The comparative câse distribution by histological
Size ol tumor
crH
RSCM (1e88-19er)
Number of
types is shown in Table 9.
(1eSe)
Number of
cases
%
CASES
Vo
TO
22
4.9
2
r82
40.8
5l
t7
191
42.8
87
29
4.7
T4
2l
156
52
30
6.7
Totals
300
r00
446
100
T1
T2
T3
6
The RSCM cases had 1.33% noninvasive carcinoma,
8833% invasive ductal carcinoma, and 9.67% special
types. The CIH cases had 7.47o noninvasive carcinoma, 80.47o invasive ductal carcinoma, and IL37o
special types. The noninvasive carcinoma group, no
lobular carcinoma in situ was found. The incidence of
noninvasive duct carcinoma is much higher at the ClH,
with a 6.O7Vo difference, than that at the RSCM.
Table 9. Histological Types and Case Distribution
The data showed that 52 7o of the Indonesian breast
cancer patients at Cipto Mangunkusumo Hospital
(RSCM) were at advanced stage with T4 size, while
such tumor was only found in 6.7Vo among the
Japanese breast cancer patients at CIH. On the contrary early breast cancers with T1 size were only seen
in2% of the Indonesian females, while it was found in
40.8% of the Japanese females.
At RSCM, the rnajority (rnore than 807o) were of
T3+T4 size, while at CIH the majority (rnore than
8O7o) were of T1+T2 size. In other words, at their
presentatiol the tumor size of breast cancer among
Indonesian females were larger than that alnong
Japanese females.
ln forty of the operable cases, the lymph node metastases could be analysed. The results are given in
Table 8.
Table 8. Case Distribution by Lymph-node Metastases
RSCM
(1e88-1eer)
CrH (lq8e)
Lympb-node metastases
Number of
cases
7o
Number of
cases
%
Negative (n0)
22
55
229
51.3
Axillary
l0
25
133
29.8
8
20
62
13.9
l5
3.4
7
1.6
1-3
(nla)
Axillary 4 or more (nlb)
Subclavicular (n2)
Supraclavicular (n3)
Totals
40
100
446
100
RSCM (1e88-1ee1) CrH (1e89)
Histological types
Number of
cases
Noninvasive carcinoma
a. Noninvasive ductal ca
b. Lobular ca in situ
Invasive carcinoma
a. lnvasive ductal ca
a1. Papillotubular
a2- Solidtubular
a3. Scirrbous
4
Mucinous ca
b2.
b3.
b4.
b5.
b6.
b7.
b8.
Medullary
ca
Invasive lobular ca
Adenoid cysticca
cases
r.33 33
4
t7
'l
1
1.33 t6
5.68 6
2.33 20
Vo
7.4
r9.3
17.5
43.6
3.6
1.3
4.5
0.33
Squamous cell ca
1
0.2
0.2
0.2
5
1.1
1
Spindle cell ca
Apocrine ca
Cla
Number of
39 13.00 86
79 26.33 78
t47 49.00 t94
b. Special types
bl.
%
1
with cartil and/or
oss. metaplasia
b9. Tubular
ca
blO.Secretory ca
(Juvenile)
Paget's disease
Tota s
07
0.67
300
100.00
445
100.0
160
Tjahjadi et al.
Med J Indones
DISCUSSION
approximately 2Vo. At the RSCM
It was of great concern, that the majority of the Indonesian breast cancers found at their presentation
were of much later stages in contrast to the Japanese
counterpart.
The earlier detection of breast caucer could be responsible for the difference shown in Table 9 for the
non-invasive types. In the invasive cârcinoma group,
the invasive ductal carcinorna is the most common,
accounting for at least 8O7o of breast cancer. The
incidence of 88.337o at the RSCM is similar with the
report of Sakamoto et al.? The scirrhous carcinoma is
the most common type of invasive ductal carcinoma,
with an incidence ol about S}Vo.rz The data of the
Indonesian breast cancers showed that the proportion
of the solid-tubular carcinoma was higher than
the
papillotubular carcinoma, while the reverse was seen
in the data of tbe Japauese breast cancer.
The sub-classification of invasive ductal carcinoma
into 3 sub-types has prognostic significance. Such
relationship has been observed by several investigators
(Sakamoto G., personal communication). The papillotubular carcinoma shows the most favorable prog-
nosis (ten-year survival rate = 77.4 %), and the
scirrhous carcinorna shows the worst prognosis (tenyear survival rate = 61.2 o/o). The solid-tubular carcinoma showed a ten-year survival rate of 64.9 7o.T\e
invasive ductal carcinorna has been referred to as
infiltrating duct carcinoma not otherwise specified
(NOS) or no special type (NST). This group of carcinoma which is usually evaluated
c grad-
ing,13' 1a which
will place th
intermediate or high grade ca
s into
This
proposed new histologic al classification can be used
instead of the grading system.
The special types of invasive breast cancer, including
mucinous carcinoma, rnedullary carcinoma, tubular
carcinoma in their pure form (more than 90o/o
homog,e.ueity) have relatively favourable prognosis.*'" Although invasive, these tumors show a low
incideuce of axillary lyrnph-nocle_lnetastases and exhibit a Iong disease free interval.r /'lu
the CIH, it is 3.67o.
itis
l.33Vo, and at
An interesting finding is that medullary carcinoma at
the RSCM has a much higher incidence rate than that
at the CIH, with a difference of 4.38%. Such type has
been considered to represent more favourable prognosis.
The incidence of lobular carcinoma in Japan is very
low and is significa_ntly different from the incidence in
Western countries./ However Sugano and Sakamoto20
found that the incidence of lobular carcinoma among
Japanese females has gradually increased. At the CIH
before 1965,the incidence was around l7o of allbreast
cancers, from l97l to 1975 it was 3.4To, and, mosl
recently, for 1974-1975, it has increased to 5.3To.They
concluded that the incidence of invasive lobular carcinoma among Japanese females is gradually approaching that of American females.
In 1989, the incidence of invasive lobular carcinoma
at CIH was 4.57o. At the RSCM, the incidence of
invasive lobular carcinoma for 1981-1985 was 1.77o
among 1265 cases of breast cancer,zr and in this study
(1989-1992), it accounted for 2.33% among 300 cases
of breast cancers.
No tubular carcinoma was found among the RSCM
cases, but 5 cases were detected among the CIH cases
of breast cancer. Tubular carcinomas are well differen-
tiated tumors which show the highest rate of cure,
among the special histologic typ;.22,23 Tubular carcinoma has received general recognition only in the
last 10 years, since it is more common in groups of
cancer detected by mammography, largely explaining
the increased interest in recent years.to This special
type of breast cancer are more frequent in prevalent
caucer (those detected at first screen by mammography) than cases detected subsequently at yearly intervals (incident cases)." Whether this is true for the
CIH cases is worthwile to be elucidatecl.
investigators estimated that special type cancer comprise lOTo of all breast cancers, while others considered
that they comprised between 25-30Vo.r6
The peak incidence ofbreast cancer among Indonesian
females was found in the 5th decade, and was similar
with the result at the CIH cases. The main difference
with reference to the age distribution of breast carcinoma between Indonesia and Japanese females was
inthe20-29 year agegroup. Thirteen cases were founcl
âmong 300 breast cancer cases at the RSCM, while
only 2 cases among Japanese females with breast cancer, in the 2O-29 year age group. It seems that breast
Mucinous carcinoma comprised_ only l-6%o of most
series of invasive breast crucer,t'and the pure type
douesian females.
In both studies (RSCM and CIH) the ilcidelce of this
special type is only about lÙt/o of the whole breast
caucer cases. This finding is similar with previous
report by Sakamoto et al.' In North America, some
cancer occurs at the younger age group
in the
In_
Vol 4, No 3, July - September 1995
Pathological Aspects of Breast
CONCLUSIONS
Cancer
16f
8. Rosen PP, Ashikari R, Thaler H, Ishikawa S, Hirota T, Abe
O, et al. A comparative study of some pathological features
of mammary carcinoma in Tokyo, Japan and New York,
USA. Ca ncer I97 7 ;39 :429 -3 4.
9. Hartmann WH, Ozello L, Sobin LH, Stalsberg H. Histological typing of breast tumoum. In : International Histological
Classification of Tumours, no 2.2nd ed. Geneva : WHO,
At younger age group QO-29 years), breast cancer had
already occured more frequently in the lndonesian
females as compared to the Japanese females. However, the age distribution in both groups peaked at ages
40-49 years. Indonesian females had larger-sized
tumors. The proportion of non-invasive carcinoma
was lower among Indonesian females, while that of
invasive ductal carcinoma was comparable in both
10. Modivitt RW, Stewart FW, Berg JW. Tumours of the breast.
ln: Atlas of Tumor Pathology. 2nd series. Washington DC:
was of great interest, that medullary carcinoma, which
11. Japanese Breast Cancer Society. The Geneial Rules for
Clinical and Pathological Recording ofBreast Cancer. Jpn J
groups. Tbe proportion of mucinous carcinoma,
lobular carcinoma were higher in Japanese females. It
has more favourable prognosis, occured
higher proportion in Indonesian females.
in much
Acknowledgments
The authors are indebted to the nurses and laboratory
technicians for excellent care of surgicopathological
specimens. This work was supported by the Ministry
of Education and Culture, Japan, Grants No.01042007
and 04042013; and was partly supported by the Indonesian Cancer Foundation. This collaborative study
was a part of Special Cancer Research Project in Monbusho International Scientific Research Program, with
the approval of the Dean, Faculty of Medicine, University of Indonesia, No. 4383 /PTO2.H4.FK / E / 88.
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Appendix
part. Comedocarcinoma belongs to this
type.
A. Principles of Classification
1.
Breast carcinoma is classified into three groups;
noninvasive ca rci noma, i nvasive ca rcinoma a nd
Paget's disease.
2.
Noninvasive carcinoma is classified into noninvasive ductal carcinoma and lobular carcinoma
in situ; Invasive carcinoma into invasive ductal
carcinoma and special types.
3.
Invasive ductal carcinoma is further classified
into three subgroups; papillotubu lar carcinoma,
solid-tubular carcinoma and scirrhous carcinoma.
Remark 1: Comedocarcinoma should be
identified as that.
Remark 2: Papillary carcinoma which is an
independent histological type in
the WHO classification has been
included in papittotubular carcinoma.
However there is still room for
further consideration.
à2. Solid+ubular
Note : since this type is characterized
by distinct bounderies, tumors
Invasive carcinoma
This group represents a carcinoma with in-
composed of medullary and/or
solid nests are also included,
vasion.
à.
carcinoma
This is a carcinoma characterized by a
solid cluster of cancer cells with expansive growth forming sharp borders.
B. Definition of Histological Types
2.
J Univ Indones
Invasive ductal carcinoma
if
This is classified into rhree subgroups;
even
cinoma and scirrhous carcinoma.
Classification of invasive carcinoma fol-
Central necrosis or fibrosis may
also be evident.
papillotubular carcinoma, solid-tubular car-
lows the rule of predominancy when there
are two or more histological patterns. In a
case where judgement of the predominant
type is difficult, the least differentiated type
should be chosen as the histological type,
with supplementary description of other histological types.
Remark 1: In practice, the predominant his-
tological type should be taken
for the principal classification,
and the secondary histological
type should be added as â sup-
plementary description.
Remark 2: The degree
of differentiation
from poor to well is in order of
scirrhous carcinorna, solidtubular carcinoma and papillotubular carcinoma.
Remark
3: A lesion with slight extraductal
invasion should be so described
for easier correspondence with
the WHO classification.
à l.
Papillotubular carcinorna
This carcinoma is characterized by
papillary projection and tubule formation, and may contain a solid pattenr in
interstitial components
of stromal tissue are
à3.
present.
Scirrhous carcinoma
Cancer cells
of this histologic
type
show scattered invasion into the stroma
in small clusters or in trabecular structures with accompanying desmoplasia
of varying degrees.
there are two subtypes. One is a pure
scirrhous carcinoma which has extremaly small amount of intraductal
component and extersive stromal invasion. The other derives from papillotubular or solid-tubular carcinoma
with a predominance of diffuse stromal
invasion.
Note :The differential diagnosis between scirrhous carcinoma and
solid-tubular carcinoma relies
on the size of cancer flests and
the fashion of infiltration at the
tumor margin. Scirrhous carcinoma is composed of small
nests, grows diffusely and infiltrates into the stromal tissue.
On the other hand, solid-tubular
carcinoma has large nests,
grows expansively and is well
circumscribed.